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Dentition and Feeding in Placodontia: Tooth Replacement in Henodus Chelyops Yannick Pommery1,2,3, Torsten M

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Dentition and Feeding in Placodontia: Tooth Replacement in Henodus Chelyops Yannick Pommery1,2,3, Torsten M Pommery et al. BMC Ecol Evo (2021) 21:136 BMC Ecology and Evolution https://doi.org/10.1186/s12862-021-01835-4 RESEARCH Open Access Dentition and feeding in Placodontia: tooth replacement in Henodus chelyops Yannick Pommery1,2,3, Torsten M. Scheyer4 , James M. Neenan5 , Tobias Reich4, Vincent Fernandez6,7 , Dennis F. A. E. Voeten6,8,9 , Adrian S. Losko10 and Ingmar Werneburg1,2* Abstract Background: Placodontia is a Triassic sauropterygian reptile group characterized by fat and enlarged crushing teeth adapted to a durophagous diet. The enigmatic placodont Henodus chelyops has numerous autapomorphic character states, including extreme tooth count reduction to only a single pair of palatine and dentary crushing teeth. This ren- ders the species unusual among placodonts and challenges identifcation of its phylogenetic position. Results: The skulls of two Henodus chelyops specimens were visualized with synchrotron tomography to investigate the complete anatomy of their functional and replacement crushing dentition in 3D. All teeth of both specimens were segmented, measured, and statistically compared to reveal that H. chelyops teeth are much smaller than the posterior palatine teeth of other cyamodontoid placodonts with the exception of Parahenodus atancensis from the Iberian Peninsula. The replacement teeth of this species are quite similar in size and morphology to the functional teeth. Conclusion: As other placodonts, Henodus chelyops exhibits vertical tooth replacement. This suggests that verti- cal tooth replacement arose relatively early in placodont phylogeny. Analysis of dental morphology in H. chelyops revealed a concave shape of the occlusal surface and the notable absence of a central cusp. This dental morphology could have reduced dental wear and protected against failure. Hence, the concave teeth of H. chelyops appear to be adapted to process small invertebrate items, such as branchiopod crustaceans. Small gastropods were encountered in the matrix close to both studied skulls. Keywords: Synchrotron tomographic scans, Functional morphology, Jaw mechanism, Ontogeny, Evolution, Triassic Background were found in Europe [4–9], in the Middle East [10], and Te extinct Sauropterygia is one of the most diversifed in Asia [11–16]. Tese remains are known from "Oberer clades of Mesozoic marine reptiles that encompasses Buntsandstein", Anisian [17, 18] to Rhaetian [19] times. pachypleurosaurs, nothosaurs, pistosaurs, plesiosaurs, Placodonts died out in or just before the Triassic-Jurassic and placodonts [1]. Placodonts are among the frst sau- extinction event (~ 201.3 Ma) without any descendants ropterygians to appear in the fossil record [1, 2]. Te frst [20]. Teir relative rarity and uncertainty regarding the material of Placodontia was described by Münster [3] exact age of several placodont-bearing deposits renders from the Bavarian Muschelkalk. Since then, its remains reconstruction of the stratigraphical and geographical distribution of Placodontia particularly challenging [21]. Nevertheless, the geological context indicates that pla- *Correspondence: [email protected] codonts inhabited shallow water near the northeastern 1 Senckenberg Centre for Human Evolution and Palaeoenvironment (HEP) an der Eberhard-Karls-Universität Tübingen, Sigwartstraße 10, and -western Tethys coastal margins [13, 21–23]. Tis 72076 Tübingen, Germany restricted geographical range may refect their specifc Full list of author information is available at the end of the article diet consisting of hard-shelled prey [24]. Placodonts © The Author(s) 2021. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http:// creat iveco mmons. org/ licen ses/ by/4. 0/. The Creative Commons Public Domain Dedication waiver (http:// creat iveco mmons. org/ publi cdoma in/ zero/1. 0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Pommery et al. BMC Ecol Evo (2021) 21:136 Page 2 of 19 feature a rather rigid body, a single pair of temporal Psephoderma, Psephochelys, and Macroplacus represent fenestrae, and a dental architecture (crushing teeth) Placochelyidae. Henodontidae consists of Henodus with adapted to a durophagous diet [21, 25]. the single species H. chelyops and the recently described species Parahenodus atancensis [8, 16, 38]. Parahenodus Placodontia dentition atancensis is represented only by a single partial cranium. Skull reconstructions across placodont diversity permits H. chelyops shares several characters with other cyamo- interspecifc comparison [24]. Besides cranial topology, dontoid placodonts, such as a short and broad carapace, the identifcation of placodont taxa also strongly relies on cranial tubercles, reducted dentition, and the separa- dental morphology (e.g., [26–29]). Te dentition of placo- tion of the nasals with Placochelyidae [24]. H. chelyops donts has been studied intensively towards understand- occurred rather late in stratigraphical deposits, which ing the variability of dental morphology and inferred may imply that this taxon is deeply nested in placodont feeding behavior across this group [2, 24, 27–33]. Tooth phylogeny but could also refect a preservation bias [36]. location, anatomy, and replacement pattern aids in phy- logenetic inferences (e.g., [29, 33]). Te dentition and the upper jaw of all major placodont groups are known for Henodus chelyops remains their good preservation and can be compared with each Henodus chelyops was frst assigned to Placodontia by v. other. Teeth are supported by the premaxilla, maxilla, and Huene in 1936 [18]. All H. chelyops remains have been palatine in the cranium, and the dentary in the mandible. discovered as well-preserved elements at one locality Paraplacodus and Placodus have long and procumbent exposing the “Oberer Gipskeuper” of the village of Lust- teeth, similar to Palatodonta bleekeri, on the premaxil- nau near Tübingen (Baden-Württemberg, Germany). lary and the anterior part of the dentary [24, 29, 34]. In Tese deposits date from the Carnian, and are com- Placodus, these chisel-shaped teeth have a deep root and posed of grey shales with thin silt laminae [18, 39, 40]. a more horizontally oriented alveolus [32]. Cyamodus Tese shales have been interpreted as being “ephemeral and Protenodontosaurus are the rare representatives of lacustrine to restricted shallow-marine” deposits [40]. H. Cyamodontoidea to bear premaxillary teeth [29, 35]. Te chelyops represents the only known placodont to have maxillary and palatine teeth, in contrast, are adapted for inhabited a brackish lagoonal environment. Several auta- crushing and feature short roots, shallow alveoli, and an pomorphic character states were described for this spe- ankylosed thecodont tooth implantation [24, 32]. Placo- cies, such as its roughly rectangular and fat skull, its chelyid placodonts have fewer teeth than other placodont wide rostrum, and its very deep and massive lower jaw [8, groups. In Placochelys and Psephoderma, as in H. chely- 18, 24, 26, 31, 36, 38, 41, 42] (Fig. 1). ops, premaxillary teeth (and antagonistic dentary coun- terparts) are absent in the narrow rostrum [24]. Henodus chelyops dentition Placodont phylogeny Te dentition of H. chelyops is extremely reduced [18, Since the end of the twentieth century, the phylogeny 24, 26, 27, 31, 41]. Te dentition of H. chelyops lacks pre- of Placodontia has been frequently addressed (e.g., [1, maxillary and maxillary teeth and involves a single pair 2, 5, 13–17, 21, 25, 34, 36]). Placodontiformes repre- of crushing teeth located across the posterior part of the sents the sister-group to all remaining sauropterygians, palatines that occludes with a corresponding pair of teeth the Eosauropterygia [37]. Placodontiformes is the group across the dentaries. Te dental antagonists on the lower that includes the non-placodont Palatodonta bleekeri as jaw are situated medially to the small coronoid processes sister taxon to Placodontia [2]. Paraplacodus is consid- on the dentary [18]. Te pair of teeth on the upper jaw is ered as sister of all remaining placodonts regarding its homologous to the posterior-most palatine teeth of other relatively plesiomorphic dentition and complete lack of placodonts [18, 31]. osteoderms in the postcranial skeleton [24, 34, 36]. Mul- Te complex of autapomorphic character states for H. tiple phylogenetic analyses converged on distinguishing chelyops has confounded inference of its phylogenetic the monophyletic clade Cyamodontoidea from the non- position within Placodontia for decades [1, 36]. Te atyp- armored placodonts Paraplacodus and Placodus [1, 5, ical ‘dentition’ of H. chelyops comprises a unique combi- 16, 34]. Cyamodontoidea is subdivided into the two taxa nation of three structures—a cutting edge with denticles, Cyamodontida and Placochelyida
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